The V-ATPase as a target for antifungal drugs

Current Protein and Peptide Science

Volumn 13, Issue 2, 2012, Pages 134-140

  Zhang, Yongqiang ^a   Rao, Rajini ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Amiodarone; Ergosterol; Fluconazole; pH; Vacuolar ATPase

Indexed keywords

AMIODARONE; AMPHOTERICIN B; ANTIFUNGAL AGENT; BLEOMYCIN; CAMPTOTHECIN; CARDIOLIPIN; CATION; CONCANAMYCIN A; CYCLOHEXIMIDE; DOXORUBICIN; FLUCONAZOLE; HYDROXYUREA; IMATINIB; PHOSPHOLIPID; PLAKORTIDE F ACID; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SPHINGOLIPID; SULFOMETURON METHYL; TAMOXIFEN; TUNICAMYCIN; UNCLASSIFIED DRUG; WORTMANNIN;

ANTIFUNGAL ACTIVITY; ANTIFUNGAL RESISTANCE; ASPERGILLUS FUMIGATUS; CANDIDA ALBICANS; CRYPTOCOCCUS NEOFORMANS; DRUG MECHANISM; DRUG POTENCY; ENZYME ACTIVITY; FUNGAL VIRULENCE; FUNGUS GROWTH; GROWTH INHIBITION; HOMEOSTASIS; MYCOSIS; NONHUMAN; PROTEIN TARGETING; REVIEW; SACCHAROMYCES CEREVISIAE; TONOPLAST;

FUNGI;

EID: 84860794492     PISSN: 13892037     EISSN: 18755550     Source Type: Journal    
DOI: 10.2174/138920312800493205     Document Type: Review

References (72)

1. Pappas, P.G.; Kauffman, C.A.; Andes, D.; Benjamin, D.K. Jr., Calandra, T.F.; Edwards, J.E. Jr., et al. Clinical practice guidelines for the management of candidiasis, 2009 update by the Infectious Diseases Society of America. Clin. Infect. Dis., 2009, 48(5), 503-535.
2. Cohen, B.E. Amphotericin B membrane action, role for two types of ion channels in eliciting cell survival and lethal effects. J. Membr. Biol., 2010, 238(1-3), 1-20.
3. Ashley, E.S.D.; Lewis, R.; Lewis, J.S.; Martin, C.; Andes, D. Pharmacology of Systemic Antifungal Agents 10.1086/504492. Clini. Infect. Dis., 2006, 43(Supplement 1), S28-S39
4. Francois, I.E.; Aerts, A.M.; Cammue, B.P.; Thevissen, K. Currently used antimycotics, spectrum, mode of action and resistance occurrence. Curr. Drug Targets, 2005, 6(8), 895-907.
5. Hitchcock, C.A.; Dickinson, K.; Brown, S.B.; Evans, E.G.; Adams, D.J. Interaction of azole antifungal antibiotics with cytochrome P-450-dependent 14 alpha-sterol demethylase purified from Candida albicans. Biochem. J., 1990, 266(2), 475-480.
6. Gudlaugsson, O.; Gillespie, S.; Lee, K.; Vande Berg, J.; Hu, J.; Messer, S.; et al. Attributable mortality of nosocomial candidemia, revisited. Clin. Infect. Dis., 2003, 37(9), 1172-1177.
7. Casey, J.R.; Grinstein, S.; Orlowski, J. Sensors and regulators of intracellular pH. Nat. Rev. Mol. Cell Biol., 2010, 11(1), 50-61.
8. Nishi, T.; Forgac, M. The vacuolar (H+)-ATPases-nature's most versatile proton pumps. Nat. Rev. Mol. Cell Biol., 2002, 3(2), 94-103.
9. Kane, P.M. The long physiological reach of the yeast vacuolar H+-ATPase. J. Bioenerg. Biomembr., 2007, 39(5-6), 415-421.
10. Dawson, K.; Toone, W.M.; Jones, N.; Wilkinson, C.R. Loss of regulators of vacuolar ATPase function and ceramide synthesis results in multidrug sensitivity in Schizosaccharomyces pombe. Eu-karyot. Cell, 2008, 7(6), 926-937.
11. dos Santos, S.C.; Sa-Correia, I. Genome-wide identification of genes required for yeast growth under imatinib stress, vacuolar H+-ATPase function is an important target of this anticancer drug. Om-ics, 2009, 13(3), 185-198.
12. Yadav, J.; Muend, S.; Zhang, Y.; Rao, R. A phenomics approach in yeast links proton and calcium pump function in the Golgi. Mol. Biol. Cell, 2007, 18(4), 1480-1489.
13. Rao, A.; Zhang, Y.; Muend, S.; Rao, R. Mechanism of antifungal activity of terpenoid phenols resembles calcium stress and inhibition of the TOR pathway. Antimicrob. Agents Chemother., 2010, 54(12), 5062-5069.
14. Staab, J.F.; Bradway, S.D.; Fidel, P.L.; Sundstrom, P. Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1. Science, 1999, 283(5407), 1535-1538.
15. [Sun, J.N.; Solis, N.V.; Phan, Q.T.; Bajwa, J.S.; Kashleva, H.; Thompson, A.; Liu, Y; Dongari-Bagtzoglou, A.; Edgerton, M.; Filler, S.G. Host cell invasion and virulence mediated by Candida albicans Ssa1. PLoS Pathog., 2010, 6(11), e1001181.
16. [Almeida, R.S.; Brunke, S.; Albrecht, A.; Thewes, S.; Laue, M.; Edwards, J.E.; Filler, S.G.; Hube, B. The hyphal-associated adhesin and invasin Als3 of Candida albicans mediates iron acquisition from host ferritin. PLoS Pathog., 2008, 4(11), e1000217.
17. Gacser, A.; Stehr, F.; Kroger, C; Kredics, L.; Schafer, W.; Nosan-chuk, J.D. Lipase 8 affects the pathogenesis of Candida albicans. Infect. Immun., 2007, 75(10), 4710-4718.
18. Mukherjee, P.K.; Seshan, K.R.; Leidich, S.D.; Chandra, J.; Cole, G.T.; Ghannoum, M.A. Reintroduction of the PLB1 gene into Candida albicans restores virulence in vivo. Microbiology, 2001, 147(Pt 9), 2585-2597.
19. [Naglik, J.R.; Challacombe, S.J.; Hube, B. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Micro-biol. Mol. Biol. Rev., 2003, 67(3), 400-428, table of contents.
20. Weissman, Z.; Shemer, R.; Conibear, E.; Kornitzer, D. An endo-cytic mechanism for haemoglobin-iron acquisition in Candida albi-cans. Mol. Microbiol., 2008, 69(1), 201-217.
21. Poltermann, S.; Nguyen, M.; Gunther, J.; Wendland, J.; Hartl, A.; Kunkel, W.; Zipfel, P.F.; Eck, R. The putative vacuolar ATPase subunit Vma7p of Candida albicans is involved in vacuole acidification, hyphal development and virulence. Microbiology, 2005; 151(Pt 5), 1645-1655.
22. Erickson, T.; Liu, L.; Gueyikian, A.; Zhu, X.; Gibbons, J.; Williamson, P.R. Multiple virulence factors of Cryptococcus neofor-mans are dependent on VPH1. Mol. Microbiol., 2001, 42(4), 1121-1131.
23. Bonilla, M.; Nastase, K.K.; Cunningham, K.W. Essential role of calcineurin in response to endoplasmic reticulum stress. Embo. J., 2002, 21(10), 2343-2353.
24. Courchesne, W.E. Characterization of a novel, broad-based fungi-cidal activity for the antiarrhythmic drug amiodarone. J. Pharmacol. Exp. Ther., 2002, 300(1), 195-199.
25. Gupta, S.S.; Ton, V.K.; Beaudry, V.; Rulli, S.; Cunningham, K.; Rao, R. Antifungal activity of amiodarone is mediated by disruption of calcium homeostasis. J. Biol. Chem., 2003, 278(31), 28831-28839.
26. Maresova, L.; Muend, S.; Zhang, Y.Q.; Sychrova, H.; Rao, R. Membrane hyperpolarization drives cation influx and fungicidal activity of amiodarone. J. Biol. Chem., 2009, 284(5), 2795-2802.
27. Muend, S.; Rao, R. Fungicidal activity of amiodarone is tightly coupled to calcium influx. FEMS Yeast Res., 2008, 8(3), 425-431.
28. Pena, A.; Calahorra, M.; Michel, B.; Ramirez, J.; Sanchez, N.S. Effects of amiodarone on K+, internal pH and Ca2+ homeostasis in Saccharomyces cerevisiae. FEMS Yeast Res., 2009, 9(6), 832-848.
29. Zhang, Y.Q.; Rao, R. Global disruption of cell cycle progression and nutrient response by the antifungal agent amiodarone. J. Biol. Chem., 2007, 282(52), 37844-37853.
30. Pozniakovsky, A.I.; Knorre, D.A.; Markova, O.V.; Hyman, A.A.; Skulachev, V.P.; Severin, F.F. Role of mitochondria in the phero-mone- and amiodarone-induced programmed death of yeast. J. Cell Biol., 2005, 168(2), 257-269.
31. Xu, T.; Feng, Q.; Jacob, M.R.; Avula, B.; Mask, M.M.; Baerson, S.R.; Tripathi, S.K.; Mohammed, R.; Hamann, M.T.; Khan, I.A.; Walker, L.A.; Clark, A.M.; Agarwal, A.K. The marine sponge-derived polyketide endoperoxide plakortide f Acid mediates its antifungal activity by interfering with calcium homeostasis. Antimicrob. Agents Chemother., 2011, 55(4), 1611-1621.
32. Parsons, A.B.; Lopez, A.; Givoni, I.E.; Williams, D.E.; Gray, C.A.; Porter, J.; Chua, G.; Sopko, R.; Brost, R.L.; Ho, C.H.; Wang, J.; Ketela, T.; Brenner, C.; Brill, J.A.; Fernandez, G.E.; Lorenz, T.C.; Payne, G.S.; Ishihara, S.; Ohya, Y.; Andrews, B.; Hughes, T.R.; Frey, B.J.; Graham, T.R.; Andersen, R.J.; Boone, C. Exploring the mode-of-action of bioactive compounds by chemical-genetic profiling in yeast. Cell, 2006, 126(3), 611-625.
33. Dolan, K.; Montgomery, S.; Buchheit, B.; Didone, L.; Wellington, M.; Krysan, D.J. Antifungal activity of tamoxifen, in vitro and in vivo activities and mechanistic characterization. Antimicrob. Agents Chemother., 2009, 53(8), 3337-3346.
34. Brett, C.L.; Kallay, L.; Hua, Z.; Green, R.; Chyou, A.; Zhang, Y.; Graham, T.R.; Donowitz, M.; Rao, R. Genome-Wide Analysis Reveals the Vacuolar pH-Stat of Saccharomyces cerevisiae. PLoS One, 2011, 6(3), e17619.
35. [Zhang, Y.Q.; Gamarra, S.; Garcia-Effron, G.; Park, S.; Perlin, D.S.; Rao, R. Requirement for ergosterol in V-ATPase function underlies antifungal activity of azole drugs. PLoS Pathog., 2010, 6(6), e1000939.
36. Gamarra, S.; Rocha, E.M.; Zhang, Y.Q.; Park, S.; Rao, R.; Perlin, D.S. Mechanism of the Synergistic Effect of Amiodarone and Flu-conazole in Candida albicans. Antimicrob. Agents Chemother., 2010.
37. Afeltra, J.; Vitale, R.G.; Mouton, J.W.; Verweij, P.E. Potent syner-gistic in vitro interaction between nonantimicrobial membrane-active compounds and itraconazole against clinical isolates of As-pergillus fumigatus resistant to itraconazole. Antimicrob. Agents Chemother., 2004, 48(4), 1335-1343.
38. Benaim, G.; Sanders, J.M.; Garcia-Marchan, Y.; Colina, C.; Lira, R.; Caldera, A.R.; Payares, G.; Sanoja, C.; Burgos, J.M.; Leon-Rossell, A.; Concepcion, J.L.; Schijman, A.G.; Levin, M.; Oldfield, E.; Urbina, J.A. Amiodarone has intrinsic anti-Trypanosoma cruzi activity and acts synergistically with posaconazole. J. Med. Chem., 2006, 49(3), 892-899.
39. Serrano-Martin, X.; Payares, G.; De Lucca, M.; Martinez, J.C.; Mendoza-Leon, A.; Benaim, G. Amiodarone and miltefosine act synergistically against Leishmania mexicana and can induce parasi-tological cure in a murine model of cutaneous leishmaniasis. An-timicrob. Agents Chemother., 2009, 53(12), 5108-5113.
40. Lin, M.; Grillitsch, K.; Daum, G.; Just, U.; Hofken, T. Modulation of sterol homeostasis by the Cdc42p effectors Cla4p and Ste20p in the yeast Saccharomyces cerevisiae. Febs J., 2009, 276(24), 7253-7264.
41. Cox, B.E.; Griffin, E.E.; Ullery, J.C.; Jerome, W.G. Effects of cellular cholesterol loading on macrophage foam cell lysosome acidification. J. Lipid Res., 2007, 48(5), 1012-1021.
42. Kato, M.; Wickner, W. Ergosterol is required for the Sec18/ATP-dependent priming step of homotypic vacuole fusion. Embo. J., 2001, 20(15), 4035-4040.
43. Baars, T.L.; Petri, S.; Peters, C.; Mayer, A. Role of the V-ATPase in regulation of the vacuolar fission-fusion equilibrium. Mol. Biol. Cell, 2007, 18(10), 3873-3882.
44. Borjihan, H.; Ogita, A.; Fujita, K.; Hirasawa, E.; Tanaka, T. The vacuole-targeting fungicidal activity of amphotericin B against the pathogenic fungus Candida albicans and its enhancement by allicin. J. Antibiot. (Tokyo), 2009, 62(12), 691-697.
45. te Welscher, Y.M.; Jones, L.; van Leeuwen, M.R.; Dijksterhuis, J.; de Kruijff, B.; Eitzen, G.; Breukink, E. Natamycin inhibits vacuole fusion at the priming phase via a specific interaction with ergos-terol. Antimicrob. Agents Chemother., 2010, 54(6), 2618-2625.
46. Lingwood, D.; Simons, K. Lipid rafts as a membrane-organizing principle. Science, 2010, 327(5961), 46-50.
47. Ryu, J.; Kim, H.; Chang, E.J.; Kim, H.J.; Lee, Y.; Kim, H.H. Pro-teomic analysis of osteoclast lipid rafts, the role of the integrity of lipid rafts on V-ATPase activity in osteoclasts. J. Bone Miner. Me-tab., 2010; 28(4), 410-417.
48. Yoshinaka, K.; Kumanogoh, H.; Nakamura, S.; Maekawa, S. Identification of V-ATPase as a major component in the raft fraction prepared from the synaptic plasma membrane and the synaptic vesicle of rat brain. Neurosci. Lett., 2004, 363(2), 168-172.
49. Dermine, J.F.; Duclos, S.; Garin, J.; St-Louis, F.; Rea, S.; Parton, R.G.; Desjardins, M. Flotillin-1-enriched lipid raft domains accumulate on maturing phagosomes. J. Biol. Chem., 2001, 276(21), 18507-18512.
50. Lafourcade, C.; Sobo, K.; Kieffer-Jaquinod, S.; Garin, J.; van der Goot, F.G. Regulation of the V-ATPase along the endocytic pathway occurs through reversible subunit association and membrane localization. PLoS One, 2008, 3(7), e2758.
51. Chung, J.H.; Lester, R.L.; Dickson, R.C. Sphingolipid requirement for generation of a funct0ional v1 component of the vacuolar AT-Pase. J. Biol. Chem., 2003, 278(31), 28872-28881.
52. Dawaliby, R.; Mayer, A. Microautophagy of the nucleus coincides with a vacuolar diffusion barrier at nuclear-vacuolar junctions. Mol. Biol. Cell, 2010, 21(23), 4173-4183.
53. Chen, S.; Tarsio, M.; Kane, P.M.; Greenberg, M.L. Cardiolipin mediates cross-talk between mitochondria and the vacuole. Mol. Biol. Cell, 2008, 19(12), 5047-5058.
54. Gary, J.D.; Wurmser, A.E.; Bonangelino, C.J.; Weisman, L.S.; Emr, S.D. Fab1p is essential for PtdIns(3)P 5-kinase activity and the maintenance of vacuolar size and membrane homeostasis. J. Cell Biol., 1998, 143(1), 65-79.
55. Dietrich, C.; Bagatolli, L.A.; Volovyk, Z.N.; Thompson, N.L.; Levi, M.; Jacobson, K.; Gratton, E. Lipid rafts reconstituted in model membranes. Biophys. J., 2001, 80(3), 1417-1428.
56. Hanson, M.A.; Cherezov, V.; Griffith, M.T.; Roth, C.B.; Jaakola, V.P.; Chien, E.Y.; Velasquez, J.; Kuhn, P.; Stevens, R.C. A specific cholesterol binding site is established by the 2.8 A structure of the human beta2-adrenergic receptor. Structure, 2008, 16(6), 897-905.
57. Pang, L.; Graziano, M.; Wang, S. Membrane cholesterol modulates galanin-GalR2 interaction. Biochemistry, 1999, 38(37), 12003-12011.
58. Pucadyil, T.J.; Chattopadhyay, A. Cholesterol modulates ligand binding and G-protein coupling to serotonin(1A) receptors from bovine hippocampus. Biochim. Biophys. Acta., 2004, 1663(1-2), 188-200.
59. Gimpl, G.; Fahrenholz, F. Cholesterol as stabilizer of the oxytocin receptor. Biochim. Biophys. Acta., 2002, 1564(2), 384-392.
60. Yao, Z.; Kobilka, B. Using synthetic lipids to stabilize purified beta2 adrenoceptor in detergent micelles. Anal. Biochem., 2005, 343(2), 344-346.
61. Thiele, C.; Hannah, M.J.; Fahrenholz, F.; Huttner, W.B. Cholesterol binds to synaptophysin and is required for biogenesis of syn-aptic vesicles. Nat. Cell Biol., 2000, 2(1), 42-49.
62. Zhang, Y.Q.; Rao, R. Beyond Ergosterol, Linking pH to Antifungal Mechanisms. Virulence, 2010, 1(6), 1-4.
63. Kinashi, H.; Someno, K.; Sakaguchi, K. Isolation and characterization of concanamycins A, B and C. J. Antibiot. (Tokyo), 1984, 37(11), 1333-1343.
64. Okoli, I.; Coleman, J.J.; Tampakakis, E.; An, W.F.; Holson, E.; Wagner, F.; Conery, A.L.; Larkins-Ford, J.; Wu, G.; Stern, A.; Ausubel, F.M.; Mylonakis, E. Identification of antifungal compounds active against Candida albicans using an improved high-throughput Caenorhabditis elegans assay. PLoS One, 2009, 4(9), e7025.
65. Tchize Ndejouong Ble, S.; Sattler, I.; Maier, A.; Kelter, G.; Men-zel, K.D.; Fiebig, H.H.; Hertweck, C. Hygrobafilomycin, a cyto-toxic and antifungal macrolide bearing a unique monoalkylmaleic anhydride moiety, from Streptomyces varsoviensis. J. Antibiot. (Tokyo), 2010, 63(7), 359-363.
66. Zhang, D.J.; Wei, G.; Wang, Y.; Si, C.C.; Tian, L.; Tao, L.M.; Li, Y.G. Bafilomycin K, a new antifungal macrolide from Streptomy-ces flavotricini Y12-26. J. Antibiot. (Tokyo), 2011.
67. Frandberg, E.; Petersson, C.; Lundgren, L.N.; Schnurer, J. Strep-tomyces halstedii K122 produces the antifungal compounds bafilomycin B1 and C1. Can. J. Microbiol., 2000, 46(8), 753-758.
68. Seto, H.; Tajima, I.; Akao, H.; Furihata, K.; Otake, N. The isolation and structures of hygrolidin amide and defumarylhygrolidin. J. An-tibiot. (Tokyo), 1984, 37(5), 610-613.
69. Del Poeta, M.; Cruz, M.C.; Cardenas, M.E.; Perfect, J.R.; Heitman, J. Synergistic antifungal activities of bafilomycin A(1), flucona-zole, and the pneumocandin MK-0991/caspofungin acetate (L-743,873) with calcineurin inhibitors FK506 and L-685,818 against Cryptococcus neoformans. Antimicrob. Agents Chemother., 2000, 44(3),739-746.
70. Xie, X.S.; Padron, D.; Liao, X.; Wang, J.; Roth, M.G.; De Braban-der, J.K. Salicylihalamide A inhibits the V0 sector of the V-ATPase through a mechanism distinct from bafilomycin A1. J. Biol. Chem., 2004, 279(19), 19755-19763.
71. Johnson R.M.; Allen, C.; Melman, S.D.; Waller, A.; Young, S.M.; Sklar, L.A.; Parra, K.J. Identification of inhibitors of vacuolar proton-translocating ATPase pumps in yeast by high-throughput screening flow cytometry. Anal. Biochem., 2010, 398(2), 203-211.
72. Kartner, N.; Yao, Y.; Li, K.; Crasto, G.J.; Datti, A.; Manolson, M.F. Inhibition of osteoclast bone resorption by disrupting vacuolar H+-ATPase a3-B2 subunit interaction. J. Biol. Chem., 2010, 285(48), 37476-37490.